Seeing via Miniature Eye Movements: A Dynamic Hypothesis for Vision

During natural viewing, the eyes are never still. Even during fixation, miniature movements of the eyes move the retinal image across tens of foveal photoreceptors. Most theories of vision implicitly assume that the visual system ignores these movements and somehow overcomes the resulting smearing. However, evidence has accumulated to indicate that fixational eye movements cannot be ignored by the visual system if fine spatial details are to be resolved. We argue that the only way the visual system can achieve its high resolution given its fixational movements is by seeing via these movements. Seeing via eye movements also eliminates the instability of the image, which would be induced by them otherwise. Here we present a hypothesis for vision, in which coarse details are spatially encoded in gaze-related coordinates, and fine spatial details are temporally encoded in relative retinal coordinates. The temporal encoding presented here achieves its highest resolution by encoding along the elongated axes of simple-cell receptive fields and not across these axes as suggested by spatial models of vision. According to our hypothesis, fine details of shape are encoded by inter-receptor temporal phases, texture by instantaneous intra-burst rates of individual receptors, and motion by inter-burst temporal frequencies. We further describe the ability of the visual system to readout the encoded information and recode it internally. We show how reading out of retinal signals can be facilitated by neuronal phase-locked loops (NPLLs), which lock to the retinal jitter; this locking enables recoding of motion information and temporal framing of shape and texture processing. A possible implementation of this locking-and-recoding process by specific thalamocortical loops is suggested. Overall it is suggested that high-acuity vision is based primarily on temporal mechanisms of the sort presented here and low-acuity vision is based primarily on spatial mechanisms.